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Neural Basis of Acquired Amusia and Its Recovery After Stroke

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Neural Basis of Acquired Amusia and Its Recovery After Stroke 8872 • The Journal of Neuroscience, August 24, 2016 • 36(34):8872–8881 Behavioral/Cognitive Neural Basis of Acquired Amusia and Its Recovery after Stroke X Aleksi J. Sihvonen,1,2 XPablo Ripolle´s,3,4 Vera Leo,2 XAntoni Rodríguez-Fornells,3,4 Seppo Soinila,5 and X Teppo Sa¨rka¨mo¨2 1Faculty of Medicine, University of Turku, 20520 Turku, Finland, 2Cognitive Brain Research Unit, Institute of Behavioural Sciences, University of Helsinki, 00014 Helsinki, Finland, 3Cognition and Brain Plasticity Group, Bellvitge Biomedical Research Institute, L’Hospitalet de Llobregat, 08907 Barcelona, Spain, 4Department of Basic Psychology, University of Barcelona, 08035 Barcelona, Spain, and 5Division of Clinical Neurosciences, Turku University Hospital and Department of Neurology, University of Turku, 20521, Turku, Finland Although acquired amusia is a relatively common disorder after stroke, its precise neuroanatomical basis is still unknown. To evaluate which brain regions form the neural substrate for acquired amusia and its recovery, we performed a voxel-based lesion-symptom mapping (VLSM) and morphometry (VBM) study with 77 human stroke subjects. Structural MRIs were acquired at acute and 6 month poststroke stages. Amusia and aphasia were behaviorally assessed at acute and 3 month poststroke stages using the Scale and Rhythm subtests of the Montreal Battery of Evaluation of Amusia (MBEA) and language tests. VLSM analyses indicated that amusia was associ- ated with a lesion area comprising the superior temporal gyrus, Heschl’s gyrus, insula, and striatum in the right hemisphere, clearly different from the lesion pattern associated with aphasia. Parametric analyses of MBEA Pitch and Rhythm scores showed extensive lesion overlap in the right striatum, as well as in the right Heschl’s gyrus and superior temporal gyrus. Lesions associated with Rhythm scores extended more superiorly and posterolaterally. VBM analysis of volume changes from the acute to the 6 month stage showed a clear decrease in gray matter volume in the right superior and middle temporal gyri in nonrecovered amusic patients compared with nona- music patients. This increased atrophy was more evident in anterior temporal areas in rhythm amusia and in posterior temporal and temporoparietalareasinpitchamusia.Overall,theresultsimplicaterighttemporalandsubcorticalregionsasthecrucialneuralsubstrate for acquired amusia and highlight the importance of different temporal lobe regions for the recovery of amusia after stroke. Key words: amusia; aphasia; music; stroke; voxel-based lesion-symptom mapping; voxel-based morphometry Significance Statement Lesion studies are essential in uncovering the brain regions causally linked to a given behavior or skill. For music perception ability, previous lesion studies of amusia have been methodologically limited in both spatial accuracy and time domain as well as bysmallsamplesizes,providingcoarseandequivocalinformationaboutwhichbrainareasunderlieamusia.Byusinglongitudinal MRI and behavioral data from a large sample of stroke patients coupled with modern voxel-based analyses methods, we were able provide the first systematic evidence for the causal role of right temporal and striatal areas in music perception. Clinically, these results have important implications for the diagnosis and prognosis of amusia after stroke and for rehabilitation planning. Introduction bilateral temporal, frontal, parietal, and subcortical networks in Functional and structural neuroimaging studies in healthy sub- the neural processing of music (Samson et al., 2010; Zatorre and jects have provided evidence for the large-scale involvement of Salimpoor, 2013; Koelsch, 2014). This evidence is, however, Received March 3, 2016; revised July 10, 2016; accepted July 12, 2016. Author contributions: A.R.-F., S.S., and T.S. designed research; A.J.S., V.L., and T.S. performed research; A.J.S., P.R., V.L., and T.S. analyzed data; A.J.S., P.R., V.L., A.R.-F., S.S., and T.S. wrote the paper. Tervaniemi, Prof. Riitta Parkkola, Prof. Taina Autti, Dr. Heli Silvennoinen, Jani Saunavaara, PhD, and radiographers This work was supported by the Academy of Finland program (1257077, 1277693), Turku University Hospital Ulla Anttalainen (†), Riku Luoto, Pentti Po¨lo¨nen, and Tuija Vahtera. We also thank the patient subjects and their Research Funding, the Finnish Brain Research and Rehabilitation Foundation, the Ella and Georg Ehrnrooth Foun- families for their participation and effort. dation, the Signe and Ane Gyllenberg Foundation, the Finnish Cultural Foundation, the National Doctoral Pro- The authors declare no competing financial interests. gramme of Psychology, the Jenny and Antti Wihuri Foundation, the Formación de Profesorado Universitario Correspondence should be addressed to Dr. Aleksi Sihvonen, Cognitive Brain Research Unit, Institute of Behav- program (AP2010-4170), and the Generalitat de Catalunya (2014 SGR1413). We thank the staffs of the HUCH ioural Sciences, Siltavuorenpenger 1 B, FI-00014 University of Helsinki, Finland. E-mail: [email protected]. Department of Neurology, Turku University Hospital Department of Neurology, and other rehabilitation hospitals in DOI:10.1523/JNEUROSCI.0709-16.2016 theHospitalDistrictofSouthwestFinlandandHelsinkimetropolitanareafortheircollaboration.WethankProf.Mari Copyright © 2016 the authors 0270-6474/16/368872-10$15.00/0 Sihvonen et al. • Neural Basis of Amusia after Stroke J. Neurosci., August 24, 2016 • 36(34):8872–8881 • 8873 largely correlational, and lesion-based studies are needed to pin- Using a large (N ϭ 77) sample of stroke patients, the aim of point which brain regions are crucial and directly related to music this exploratory combined VLSM-VBM study was to determine processing. Amusia is a neural disorder characterized by severe the specific lesion patterns associated with acquired amusia and impairment of music perception and/or production caused by with changes in GM volume (GMV) and WM volume (WMV) abnormal brain development (congenital amusia) or brain dam- related to amusia recovery in a 6 month follow-up. age (acquired amusia). Deficit in perceiving fine-grained pitch changes is the hallmark symptom of amusia, but also other do- Materials and Methods mains of music, such as rhythm, can be affected (Stewart et al., Subjects and study design. Subjects (N ϭ 77) were stroke patients enrolled 2006). in two music intervention studies in Helsinki and Turku. Fifty patients Although acquired amusia is relatively common after stroke were recruited during 2004–2006 from the Department of Neurology of (ranging from 35 to 69%; Ayotte et al., 2000; Schuppert et al., the Helsinki University Central Hospital (HUCH) and 27 patients during 2000; Sa¨rka¨mo¨ et al., 2009), the exploration of its neuroanatomi- 2013–2014 from the Department of Neurology of the Turku University cal basis has been limited to symptom-led and lesion-led studies Hospital. All of the patients had an MRI-verified acute ischemic stroke or of individual cases or small (N Յ 20) patient groups. Acquired intracerebral hemorrhage in the left or right hemisphere, primarily in middle cerebral artery (MCA) territory, had cognitive or motor deficits, amusia has been associated with damage to different temporal, and were right-handed. All patients had normal hearing. Patients with frontal, parietal, and subcortical regions (Stewart et al., 2006), but prior neurological or psychiatric disease or substance abuse were not results regarding lesion lateralization (left/right) and type of mu- included. Demographic and clinical characteristics of the patients are sical deficit have been mixed, with some studies reporting spec- presented in Table 1. The individual studies were approved by the Ethics tral (e.g., pitch) or temporal (e.g., rhythm) deficits mainly after Committees of the Hospital District of Helsinki and Uusimaa and of the right hemisphere damage (Kester et al., 1991; Rosslau et al., 2015) Hospital District of Southwest Finland. Studies were performed in or after both left and right hemisphere damage (Lie´geois-Chauvel conformance with the Declaration of Helsinki. All patients signed an et al., 1998; Ayotte et al., 2000; Schuppert et al., 2000). Overall, informed consent and received standard stroke treatment and rehabili- tation. All participants underwent a behavioral assessment and an MRI constrained by small sample sizes and low spatial accuracy, these within 3 weeks of the stroke. Behavioral assessment was repeated during studies provide only coarse information about which specific the follow-up at 3 months and MRI was repeated at 6 months poststroke. brain areas are crucial for perceiving the different elements of Behavioral assessment. Music perception was evaluated by using a music. shortened version (Sa¨rka¨mo¨ et al., 2009) of the Montreal Battery of Eval- Voxel-based lesion-symptom mapping (VLSM) is a method uation of Amusia (MBEA; Peretz et al., 2003) at the acute stage (Ͻ3 weeks for analyzing the relationship between focal brain damage and after stroke) and at the 3 month poststroke stage as a part of a larger behavior by using the same voxel-based procedures used in ana- neuropsychological testing battery. We used the MBEA Scale and lyzing functional neuroimaging data (Bates et al., 2003). Com- Rhythm subtests as indices of musical pitch and rhythm perception, pared with traditional lesion analysis methods, VLSM is more respectively, and their average score as an overall index of music percep- tion (referred to hereafter as MBEA total score; Sa¨rka¨mo¨ et al., 2009).
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